Sexual Maturity & Histological Alterations of Nile Tilapia (PDF)

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OPEN ACCESS https://scidoc.org/IJAAP.php International Journal of Anatomy & Applied Physiology (IJAAP) ISSN 2572-7451 Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic Research Article Mehrim AI*, Khalil FF, Hassan ME Faculty of Agriculture, Animal Production Department, Mansoura University, Mansoura, Egypt. Abstract The accelerated growth of aquaculture industry in the past decades has resulted in environmental damages and low pro- ductivity of various aquatic organisms including fish, which seriously need for increased using of dietary probiotics in aquaculture practices. Thus, the present study was conducted to evaluate the effects of the graded levels of a newly dietary probiotic Hydroyeast Aquaculture® on morphological, anatomical of sexual maturation and histological characteristics of the gonads of both sexes of adult Nile tilapia, Oreochromis niloticus for 8 weeks. A total of 240 fish (120 males and 120 females) were separately distributed into eight homogeneous treatments as 0 (T1, as a control), 5 (T2), 10 (T3), and 15 g Hydro yeast Aquaculture® Kg1 diet (T4) for males and the same levels of tested probiotic (T5 as a control, T6, T7, and T8) are being for females. The obtained results revealed that both fish sexes fed the different levels of tested probiotic achieved the positively effects on the gonads morphological, anatomical and histological forms compared to fish fed diet free probiotic. Based on the obtained results, it could be concluded the valuable addition of 15 g Kg1 diet (T4) and 10 g Kg1 diet (T7) of Hydroyeast Aquaculture® for adult O. niloticus males and females, respectively to enhance the morphological, anatomical of sexual maturation and histological characteristics of the gonads, which consequently lead to realize the sustainability and increase the profitability in the fish hatcheries. Keywords: Aquaculture; Probiotic; Feed Additives; Nile Tilapia; Fish Reproduction. Abbreviations: GAFRD: General Authority for Fish Resources Development; BD: Basal Diet; CFU: Colony Forming Units; H: Hematoxyline; E: Eosin; SCY: Spermatocytes; YG: Yolk Globules; YV: Yolk Vesicles; SPZ: Spermatozoa. Introduction Particularly, Nile tilapia, Oreochromis niloticus is one of the most produced and economic freshwater fish species not only in the Aquaculture is a highly economic yield projects, if achieved worldwide, but also in Egypt. Where, the latest Egyptian statistics correctly. It is the fastest growing production sector all over of fish production revealed that tilapias are considered as the the world. Where, it's the world wealth coming expansion to major cultured species; they contributed about 74.52% (875.5 reimburse the shortage in animal protein. Globally, total fish metric tonnes) of the total aquaculture production (1174.8 metric production peaked at about 171 million tonnes in 2016, where tonnes). The adaptability to a wide environmental and dietary total aquaculture production has grown extremely during the last conditions justifies their success. The expected population growth fifty years from a production of less than a million tonne in the requires the development of more efficient and productive food early 1950s to 80.0 million tonnes (54.1 million tonnes of finfish, production systems. Although tilapia presents the good 17.1 million tonnes of molluscs, 7.9 million tonnes of crustaceans supra cited attributes for aquaculture, the intensification of and 938.5 metric tonnes of other aquatic animals) by 2016. This the production can be associated with the sufficient of fry by level of aquaculture production had a value of US$ 232 billion. improving the reproductive performance. Tilapias are among the most produced farmed fish in the world. Feeds play an imperative role in both of the practical and economic aspects of the fish production cycle. Feed additive sectors are *Corresponding Author: Ahmed I. Mehrim, Faculty of Agriculture, Animal Production Department, Mansoura University, 35516 Mansoura, Egypt. Tel: +201002915069 E-mail: [email protected] Received: December 24, 2018 Accepted: January 23, 2019 Published: January 28, 2019 Citation: Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. doi: http://dx.doi.org/10.19070/2572-7451-1900019 Copyright: Mehrim AI© 2019. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited. Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. 103 OPEN ACCESS https://scidoc.org/IJAAP.php growing day after day to realize the better growth and health for not included the reproductive performance in pre-spawning or fish and shrimp, as well as to meet the potential requirements spawning stages of the fish. Moreover, in our knowledge not of the fish farmers. Feed additives may be both nutritive and any research was focused on the effect of probiotics on the non-nutritive ingredients and work by either direct or indirect morphological, anatomical and histological traits of the fish methods on the animal’s system [6, 7]. Currently, there are more gonads in the pre-spawning stage, as the potential biological sustainable ways to improve the health and performance of tilapia indicators for the reproductive performance of broodstock in by complementing feeds with functional foods. Functional the spawning period. Consequently, the objectives of the present feed additives are available to regulate growth performance and study were unique to evaluate the effects of the graded levels of a health of cultivated fish, improve their immune systems, induce newly commercial dietary probiotic Hydroyeast Aquaculture® for physiological benefits, and led to improve aquaculture profit 8 weeks on both sexes of adult Nile tilapia O. niloticus (in the pre- beyond traditional feeds. These functional feed additives including spawning stage), concerning their morphological, anatomical of probiotics, prebiotics, immunostimulants, phytogenic substances, sexual maturation and histological characteristics of the gonads. enzymes, mycotoxin binders and organic acids [6, 9]. Materials and Methods Current strategies can include diet supplementation with probiotics or ‘live organisms that, when administered in acceptable The Experimental Management amounts, confer a health benefit on the host’. Probiotics are very promising in animal production, especially in aquaculture, Both sexes of adult Nile tilapia, O. niloticus with an average initial given the abundance of pathogen and other antigenic stimulus body weight (83.4 ± 0.001 g) for males and (80.1 ± 0.002) for in aquatic environment and their intimate contact with the females. Fish were purchased from the Integrated Fish Farm at animals. Using of probiotics is an imperative management Al-Manzala (General Authority for Fish Resources Development tool in aquaculture sector, but their effectiveness depends on (GAFRD) – Ministry of Agriculture) Al-Manzala, Al-Dakhalia understanding the nature of competition between species or Governorate, Egypt. Fish were stocked into a rearing tank for strains. Probiotics exhibited promising application in aquaculture, two weeks as an adaptation period, during that fish were fed a but still needs extensive attempts of research. Many commercial basal diet (BD). A total of 240 fish (120 males and researches were increasable conducted into the use of probiotics 120 females) were separately distributed into eight homogeneous for aquaculture with the demand for environment-friendly treatments (as three replicates (tanks) per treatment, Table 1). sustainable aquaculture1. Furthermore, nowadays probiotics are Fish were stocked at 10 fish m3 per tank. Each tank (1m3 in quite commonplace in health promoting “functional foods” volume) was supplied with an air stone connected to an electric for humans, as well as therapeutic, prophylactic and growth compressor. Waste was removed from each tank by siphoning, supplements in animal production and human health [13, 14]. then fresh underground water was used to change one third of Where, the method of probiotic establishment can be summarized the water every day. in three steps, attraction, association into the surface secreting gel and ended by attachment to animal tissue cells. The tested probiotic, Hydroyeast Aquaculture® formula was comprised of oligosaccharides (50,000 ppm); enzymes (amylase Probiotics demonstrated their successes in human and animal 3.7 × 106, protease 5 × 105, cellulose 2 × 105, pectinase 1 × feeding practices and recently gained attention in aquaculture. 105, xylanase 1 × 104, phytase 3 × 103 units Kg1); live yeast (5 Thus, several types of dietary probiotics were used of different × 1012 colony forming units (CFU) Kg1); and probiotics bacteria fish species, partially in O. niloticus for improving the growth (Lactobacillus acidophilus, Bifedobacterium longhum, B. thermophylu, and performance [16, 17], water quality [18, 19], physiological [20, 21], Streptococcus faecium 22.5 × 108 CFU Kg1 for each). It was produced and immune responses [4, 22], and intestinal morphology [23, 24]. by Agranco corp., Gables, International Plaza Suite, No. 307, However, few attempts have been attentive on the possible role of 2655 Le Jeune Rd., 3rd Floor, Coral Gables, Fl 33134, USA. probiotic on the reproductive development with special emphasis to the marine or ornamental fish [26-28]. Whereas the effects The commercial BD used in the present study contains 25% crude of probiotics on freshwater fish species have been investigated to a protein, which was purchased from Al-Manzala manufacture for limited extent [29, 30]. Although, many applications of probiotics fish feed, the Integrated Fish Farm at Al-Manzala (GAFRD - in aquaculture more recently documented by Dawood et al., Ministry of Agriculture), Al-Dakhalia Governorate, Egypt. The Table 1. Details of the experimental treatments. Treatment Details T1, ♂ Basal diet (BD) + 0.0 g Hydroyeast Aquaculture® Kg1 diet (as a control) T2, ♂ Basal diet (BD) + 5.0 g Hydroyeast Aquaculture® Kg1 diet T3, ♂ Basal diet (BD) + 10.0 g Hydroyeast Aquaculture® Kg1 diet T4, ♂ Basal diet (BD) + 15.0 g Hydroyeast Aquaculture® Kg1 diet T5, ♀ Basal diet (BD) + 0.0 g Hydroyeast Aquaculture® Kg1 diet (as a control) T6, ♀ Basal diet (BD) + 5.0 g Hydroyeast Aquaculture® Kg1 diet T7, ♀ Basal diet (BD) + 10.0 g Hydroyeast Aquaculture® Kg1 diet T8, ♀ Basal diet (BD) + 15.0 g Hydroyeast Aquaculture® Kg1 diet Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. 104 OPEN ACCESS https://scidoc.org/IJAAP.php commercial BD is consisted of some ingredients such as yellow compared to the control treatment free from the tested probiotic corn, rice bran, soybean meal (44%), fish meal (65%), salts, (T5). calcium carbonate, vegetable oil, vitamins and minerals premix, Di-nitro bio (Anti oxidant) and Bintonite (as banding agent) Anatomical of Secondary Sexual Maturation Characteristics according to the manufacture's formula. The commercial diet was ground to add the different levels of tested probiotic, Hydroyeast Male: Anatomically, the sexual maturation signs of adult males Aquaculture® as shown in Table 1, and then all diets were re- O. niloticus at the end of the experiment (8th week) were illustrated pelleted. The experimental diets were introduced manually twice in Figure 3 (a, b, c and d), which showed the biggest testis in daily at 9.0 am and 15.0 pm into 3% of the fish total biomass. T4, T3 and T2 compared to the control group (T1). These signs reflected the positive effects of dietary supplementation of the Secondary Sexual Maturation Characteristics graded levels of the tested probiotic, especially in T4 compared to the control treated diet free from the tested probiotic (T1). Five males and five females of O. niloticus in each treatment were randomly chosen and anaesthetized by transferring into a Female: The sexual maturation signs of adult females O. niloticus small plastic tank containing 10L water supplemented with 3mL at the end of the experiment were illustrated in Figure 4 (a, b, pure clove oil (dissolved in 10mL absolute ethanol). Then, the c and d), which showed maturation green-yellowish eggs in fish secondary sexual maturation charsteristics were recorded by digital ovaries especially in T7 followed by T6 and T8 compared to the camera after four weeks and at the end of the experiment (8th control group (T5). These signs reflected the positive effects of week). However, the anatomical observations of both sexes were dietary graded levels of tested probiotic especially in T7 compared recorded only at the end of the experiment. Where, both fish sexes to the control diet free from the tested probiotic (T5). were anaesthetized and sacrificed for the anatomical examination. The digital camera was used for recording the secondary sexual Histological Examination of the Gonads maturation and anatomical signs in the experimental fish, CASIO, Exilim optical 3x, 6.0 Mega pixels, 2.5" LCD, Anti-shake DSP, Testes: Testes of adult males O. niloticus fed BD only (T1, as a CASIO Computer Co., LTD., Tokyo, Japan. control) showed normal structure of seminiferous tubules filed with spermatocytes (scy) (Figure 5a). Yet, dietary supplementation Gonads Histological Examinations of 5g Hydroyeast Aquaculture® probiotic Kg1 diet (T2) showed normal structure of seminiferous tubules filed with scy and At the end of the experiment (8th week), fish males and females spermatids (st) (Figure 5b), which cleared by microscopic high were anaesthetized by the same above anesthetic and sacrificed, magnification (Figure 5c). However, adult males O. niloticus fed where the target organs (gonads) were sampled. Samples were 10 g probiotic Kg1 (T3) showed normal structure of seminiferous fixed in 10% neutralized formalin solution followed by washing tubules, lumen which, filed with scy and st (Figure 5d), whereas in with tab water, then dehydrated by different grades of alcohol (70, the same treatment (T3), microscopic high magnification revealed 85, 96 and 99%). Samples were cleared by xylene and embedded clearly scy and st within the lumen of seminiferous tubules (Figure in paraffin wax. The wax blocks were sectioned to six microns. 5e). Meanwhile, fish fed probiotic at level of 15 g Kg1 diet (T4) The sections were stained by hematoxyline (H) and eosin (E), and showed normal structure of semineferous tubules, lumen filed then subjected to a histological examination for gonads (testis and with scy and st and interstitial tissue (Figure 5f). Also, by high ovaries) according to Roberts. magnification in the same treatment (T4) showed spermatozoa (spz) absolutely, cleared in the lumen of seminiferous tubules Results (Figure 5g). Thus, it could be noted that all of these histological development in testis of experimental fish due to dietary Morphological of Secondary Sexual Maturation supplementation of tested probiotic. Characteristics Ovary: The histological examination in ovaries of adult females Male: Morphologically, the secondary sexual maturation signs of O. niloticus fed BD (as a control, T5) showed normal structure adult males O. niloticus at the 4th week were illustrated in Figure 1 of ovarian lamellae, which contains oocytes at various stages of (a, b, c and d); while Figures (e, f, g and h) showed these signs at oogenesis (Figure 6a), as well as, in the same treatment (T5) by the 8th week (the end of the experiment), which were appeared as high magnification Figure (6b) showed oocytes in primary stage. dispersing the red color patches on the ventral side, pectoral fins However, fish fed Hydroyeast Aquaculture® probiotic at level of and caudal fin. These signs gradually increased by adding graded 5 g Kg1 (T6) showed normal structure of ovarian lamellae, which levels of the tested Hydroyeast Aquaculture® probiotic especially contains oocytes at various stages of oogenesis and oocytes in in T4 (15g probiotic Kg1 diet) compared to the control treatment yolk vesicles (YV) stage (Figure 6c). Yet, fish fed dietary probiotic free inclusion of tested probiotic (T1). at level of 10 g Kg1 (T7) showed oocytes in yolk globules (YG) and YV stages (Figure 6d). From other hand, fish fed 15 g probiotic Female: The secondary sexual maturation signs of adult females Kg1 diet (T8) showed oocytes in late vitellogenic stage (Figure 6e) O. niloticus at the 4th week were illustrated in Figure 2 (a, b, c and and in ripening stage (Figure 6f). d); while Figures (e, f, g and h) showed these signs at the end of the experiment (8th week), which were appeared as increasing the Discussion abdomen, project the genital orifice and the eggs emerged from it. These signs gradually increased by adding the graded levels Sexual dimorphic characteristics vary, but color patterns are useful of the tested probiotic especially in T7 (10 g probiotic Kg1 diet) to differentiate some, and urogenital features permit the sexing of Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. 105 OPEN ACCESS https://scidoc.org/IJAAP.php Figure 1. Secondary sexual maturation signs (arrows) of adult males O. niloticus, (a) T1 as a control; (b) T2; (c) T3 and (d) T4 at the 4th week, and (e), (f), (g) and (h) at the 8th week of the experiment. Figure 2. Secondary sexual maturation signs (circles) of adult females O. niloticus, (a) T5 as a control; (b) T6; (c) T7 and (d) T8 at the 4th week, and (e), (f), (g) and (h) at the 8th week of the experiment. Figure 3. Testes anatomical signs (arrows) of adult males O. niloticus at the 8th week of the experiment, (a) T1 as a control; (b) T2; (c) T3 and (d) T4. Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. 106 OPEN ACCESS https://scidoc.org/IJAAP.php Figure 4. Ovaries anatomical signs (arrows) of adult females O. niloticus at the 8th week of the experiment, (a) T5 as a con- trol; (b) T6; (c) T7 and (d) T8. Figure 5. Transverse section in testes of adult O. niloticus, (a): fed BD (T1, control) (× 100, H&E stains); (b): fed 5g probi- otic Kg1 diet (T2) (× 100, H&E stains); (c): High magnification of T2 (b) (× 400, H&E stains); (d): fed 10g probiotic Kg1 diet (T3) (× 100, H&E stains); €: High magnification of T3 (d) (× 400, H&E stains); (f): fed 15g probiotic Kg1 diet (T4) (× 100, H&E stains); (g): High magnification of T4 (f) (× 400, H&E stains). Figure 6. Transverse section in ovary of adult O. niloticus (a): fed BD (T5, control) (× 80, H & E stains); (b): High magni- fication of T5 (× 160, H & E stains); (c) fed 5g probiotic Kg1 diet (T6) (× 160, H & E stains); (d): fed 10g probiotic Kg1 diet (T7) (× 400, H & E stains); €: fed 15g probiotic Kg1 diet (T8) (× 400, H & E stains). Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. 107 OPEN ACCESS https://scidoc.org/IJAAP.php adult fish. The papilla of males is slightly larger, more pointed, and has a single terminal urogenital opening, whereas the papilla Based on the histological findings of ovaries in the present study, of the female has a subterminal urinary pore and a horizontal slit fish fed graded levels of the tested probiotic, especially in T7 (10 like genital opening midway between the tip and anus. Present g Kg1 diet). The superiority of this treatment related with its findings of morphological sexual maturation characteristics of respectable reproductive physiological results, concerning the adult males and females' O. niloticus increased gradually by dietary highest serum progesterone, egg diameter, and highest fecundity tested probiotic especially in T4 and T7 respectively, compared to of adult females' O. niloticus previously stated by Mehrim et al., the control treatments (T1 & T5) at 4th week or at 8th week, as well. This advantage of T7 among other treatments also may be as anatomical sexual maturation signs at 8th week, which reflected related with the role of tested Hydroyeast Aquaculture® probiotic the maturation of gonads and highly related with the reproductive to enhance host enzyme secretion which, increase the digestive physiological findings reported in a complementary study to the efficacy of the complex proteins and lipids included in the diet present study by Mehrim et al.,. thus, increasing feed digestion and absorption by the host. These findings are strongly agreement with those reported by Tovar In all the Oreochromis spp. males grow faster and to a larger size than et al., and Ghosh et al., [26, 44]. Since, there were positive females. This difference in growth is pronounced after the onset correlation between the presence of proteins and fatty acids in the of sexual maturity, and several factors are considered relevant ; brood stock diet and reproductive-related factors such as better as the importance of territory in reproductive strategy, which may oocyte development and maturation, higher rate of vitellogenesis have favored the selection of larger males; the anabolic effects of and larger egg size [26, 45]. Moreover, Abasali and Mohamad androgens; the greater energy requirement for egg formation than also reported that the commercial probiotic (Primalac®) could be for testicular development; the lack of feeding during brooding enhanced the reproductive performance of platy-fish broodstock by females. In adult tilapia males the genital papilla has only one Xiphophorus maculates during different reproductive stages. opening (the urinary pore of the urethra) through which both milt (sperm) and urine pass. However, in females the eggs exit In the present study, the histological examination of adult through a separate oviduct and only urine passes through the females' O. niloticus ovaries revealed the presence of different urinary pore. Examination of the genital opening can therefore be development stages of oocytes (Figure 6 a-f). These observations used to determine the sex of tilapia, once a size of approximately were accordingly with those reported by Wallace ; West 30 gram is reached. Moreover, the description of stages. Whereas, major developmental events can be divided into provides information about the extension of the gonad in six phases: oogenesis, primary oocyte growth, cortical alveolar relation to the body cavity as well as the width of the gonad at the stage, vitellogenesis, maturation and ovulation. Oocytes of widest point. Relative size, shape, consistency and structure are all developmental stages were found throughout the reproductive the most important characteristics distinguishing maturity stages. cycle indicating that T. zillii possess asynchronous ovaries. Differences in colour between maturity stages that occur during Oocytes undergo the same basic pattern of growth in all teleost development due to yolk and sperm formation. The colour is a species studied. Even within an individual oocyte, there are likely more prominent trait in females than males, as the variation in to be periods when these growth phases overlap. Moreover, colour between testes in different maturity stages is subtler than even in synchronous ovaries, two or three phases may occur for ovaries. simultaneously , where similar structures were also reported by Hussein. Likewise, the microscopic criteria applied in Gonadal development is a continuous process, but specific the classification of ovarian development are based on oocyte histological characteristics can be used to classify stages of gonadal characteristics such as the formation of cortical alveoli, degree of development during the reproductive cycle. Thus, several yolk accumulation and nuclear migration. stages of spermatogenesis in adult males' O. niloticus (spermatocytes, spermatid and spermatozoa) in the present study similar with those The immunostimulatory effects of several feed additives differ by reported by Msiska. In addition, secondary spermatocytes fish species, route of management, dose, duration and association were illustrated by darkly staining chromatin as in other teleost with other immunostimulants were intensively reported fish. Meanwhile, spermatozoa were concentrated in the lumen. Generally, the obtained results herein revealed that the [37, 38]. In the seminiferous epithelium, spermatogenesis takes probiotic incorporated diets helped to increase the reproductive place within cysts or spermatocysts that are formed when a single performance and gonads maturation of the both sexes of adult spermatogonia (primary or type A spermatogonia) is completely O. niloticus. Where, the stimulatory role of tested probiotic on enveloped by Sertoli cells [39, 40]. Spermatogenesis is a complex appearance the morphological and anatomical alterations and biological process of cellular transformation that produces male enhancement the histological structure of gonads of both sexes O. haploid germ cells from diploid spermatogonial stem cells [41, niloticus may be due to both the activation of the neuroendocrine 42]. From the histological point of view, at the present study, system that regulates the reproduction process and to local factors several stages of spermatogenesis were detected in adult males' that control oocyte development and maturation. These findings O. niloticus fed dietary tested probiotic especially T4 compared are in agreement with those obtained by Ghosh et al., who to the control (T1) group (Figure 5 a-g), which highly associated reported that using 106–108 cells of Bacillus subtilis g1 diet increased with the morphological sexual maturation characteristics (Figure the reproductive performance parameters and production of fry 1 a-h) and anatomical sexual maturation signs of testes (Figure from the females of four species of ornamental fishes. Thus, 3 a-d). Similarly, these findings are also strongly related with the these authors proposed that complex B vitamins synthesized by significantly increased of total testosterone, testes weight, gonado the probiotic, especially thiamine (vitamin B1) and vitamin B12, somatic index, sperm quality parameters of adult males' O. niloticus contribute to reduce the number of dead or deformed offspring. fed Hydroyeast Aquaculture® probiotic reported by Mehrim et Moreover, Abasali and Mohamad stated that significant al.,. differences between the control and probiotic-treated groups Mehrim AI, Khalil FF, Hassan ME. Sexual Maturity Signs and Histological Alterations of Adult Oreochromis Niloticus (Linnaeus, 1758) Fed Probiotic. Int J Anat Appl Physiol. 2019;5(1):103-110. 108 OPEN ACCESS https://scidoc.org/IJAAP.php of X. helleri; in the total production of fries per female and the Fish Statistics Yearbook 2015. 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